Effect of ischaemic preconditioning on hepatic oxygenation, microcirculation and function in a rat model of moderate hepatic steatosis

Clinical Science

Volumn 108, Issue 1, 2005, Pages 55-63

  Koti, Rahul S ^a   Yang, Wenxuan ^a   Glantzounis, Georgios ^a   Quaglia, Alberto ^b   Davidson, Brian R ^a   Seifalian, Alexander M ^a  

^a ROYAL FREE AND UNIVERSITY COLLEGE MEDICAL SCHOOL   (United Kingdom)

^b ROYAL FREE HOSPITAL   (United Kingdom)

Author keywords

Hepatocellular injury; Ischaemia reperfusion injury; Ischaemic preconditioning; Liver; Steatosis

Indexed keywords

ADENOSINE TRIPHOSPHATE; ALANINE AMINOTRANSFERASE; ASPARTATE AMINOTRANSFERASE; LIVER ENZYME;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENZYME BLOOD LEVEL; FATTY LIVER; HEART INFARCTION PREVENTION; HEMODYNAMICS; HISTOLOGY; LAPAROTOMY; LASER DOPPLER FLOWMETRY; LIVER CELL DAMAGE; LIVER FUNCTION; LIVER INJURY; MALE; MICROCIRCULATION; MUSCLE ISCHEMIA; NEAR INFRARED SPECTROSCOPY; NONHUMAN; OXIDATION REDUCTION REACTION; PRIORITY JOURNAL; RAT; REPERFUSION INJURY; TISSUE OXYGENATION;

ADENOSINE TRIPHOSPHATE; ANIMALS; FATTY LIVER; LIVER; MALE; MICROCIRCULATION; MODELS, ANIMAL; OXIDATION-REDUCTION; RATS; RATS, SPRAGUE-DAWLEY; REPERFUSION INJURY;

EID: 11144222677     PISSN: 01435221     EISSN: None     Source Type: Journal    
DOI: 10.1042/CS20040130     Document Type: Article

References (56)

1. Makuuchi, M., Mori, T., Gunven, P., Yamazaki, S. and Hasegawa, H. (1989) Safety of hemihepatic vascular occlusion during resection of the liver. Surg. Gynecol. Obstet. 130, 824-831
2. Todo, S., Demetris, A. J., Makowka, L. et al. (1989) Primary nonfunction of hepatic allografts with preexisting fatty infiltration. Transplantation 47, 903-905
3. Adam, R., Reynes, M., Johann, M. et al. (1991) The outcome of steatotic grafts in liver transplantation. Transplant Proc. 23, 1538-1540
4. Seifalian, A. M., Piasecki, C., Agarwal, A. and Davidson, B. R. (1999) The effect of graded steatosis on flow in the hepatic parenchymal microcirculation. Transplantation 68, 780-784
5. Fukumori, T., Ohkohchi, N., Tsukamoto, S. and Satomi, S. (1997) Why is fatty liver unsuitable for transplantation? Disorientation of mitochondrial ATP synthesis and sinusoidal structure during cold preservation of a liver with steatosis. Transplant Proc. 29, 412-415
6. Nakano, H., Nagasaki, H. and Barama, A. (1997) The effect of N-acetylcysteine and anti-intracellular adhesion molecule-I monoclonal antibody against ischemia-reperfusion injury of the steatotic liver produced by a choline-methionine-deficient diet. Hepatology 26, 670-678
7. Selzner, M., Rudiger, H. A., Sindram, D., Madden, J. and Clavien, P. A. (2000) Mechanisms of ischemic injury are different in the steatotic and normal rat liver. Hepatology 32, 1280-1288
8. Hilden, M., Christoffersen, P., Juhl, E. and Dalgaard, J. B. (1977) Liver histology in a 'normal' population: examinations of 503 consecutive fatal traffic casualties. Scand. J. Gastroenterol. 12, 593-597
9. Underwood, G. K. (1984) Prevalence of fatty liver in healthy male adults accidentally killed. Aviat. Space Environ. Med. 55, 59-61
10. Alpers, D. H., Sabesin, S. M. and White, H. M. (1993), Fatty liver: biochemical and clinical aspects. In: Diseases of the Liver (Schiff, E. and Schiff, E. R., eds.), pp. 825-855, J. B. Lippincott, Philadelphia
11. Burt, A. D., Mutton, A. and Day, C. P. (1998) Diagnosis and interpretation of steatosis and steatohepatitis. Semin. Diag. Pathol. 15, 246-258
12. Ijaz, S., Yang, W., Winslet, M. C. and Seifalian, A. M. (2003) Impairment of hepatic microcirculation in fatty liver: a review. Microcirculation 10, 447-456
13. Chui, A. K., Haghighi, K., Painter, D. et al. (1998) Donor fatty (steatotic) liver allografts in orthotopic liver transplantation. Transplant Proc. 30, 3286-3287
14. De, C. L., Sansalone, C. V., Rondinara, G. F. et al. (1996) Is the use of marginal donors justified in liver transplantation? Analysis of results and proposal of modern criteria. Transpl. Int. 9, S414-S417
15. Fishbein, T. M., Fiel, M. I., Emre, S. et al. (1997) Use of livers with microvesicular fat safely expands the donor pool. Transplantation 64, 248-251
16. Lemasters, J. J., Bunzendahl, H. and Thurman, R. G. (1995) Reperfusion injury to donor livers stored for transplantation. Liver. Transpl. Surg. 1, 124-138
17. Trevisani, F., Colantoni, A., Caraceni, P. and Van Thiel, D. H. (1996) The use of donor fatty liver for liver transplantation: a challenge or a quagmire? J. Hepatol. 24, 114-121
18. Serafin, A., Rosello-Catafau, J., Prats, N., Xaus, C., Gelpi, E. and Peralta, C. (2002) Ischemic preconditioning increases the tolerance of fatty liver to hepatic ischemia-reperfusion injury in the rat. Am. J. Pathol. 161, 587-601
19. Murry, C. E., Jennings, R. B. and Reimer, K. A. (1986) Preconditioning with ischemia: a delay of lethal cell injury in ischemic myocardium. Circulation 74, 1124-1136
20. Koti, R. S., Seifalian, A. M. and Davidson, B. R. (2003) Protection of the liver by ischemic preconditioning: a review of mechanisms and clinical applications. Digest. Surg. 20, 383-396
21. Koti, R. S., Yang, W., McBride, A. G., Seifalian, A. M. and Davidson, B. R. (2002) The relationship of hepatic tissue oxygenation with nitric oxide metabolism in ischemic preconditioning of the liver. FASEB J. 16, 1654-1656
22. Koti, R. S., Yang, W., Dashwood, M. R., Davidson, B. R. and Seifalian, A. M. (2002) The effect of ischemic preconditioning on hepatic microcirculation and function in a rat model of ischemia reperfusion injury. Liver Transplant. 8, 1182-1191
23. Cutrin, J. C., Perrelli, M.-G., Cavalieri, B., Peralta, C., Rosselo-Catafau, J. and Poli, G. (2002) Microvascular dysfunction induced by reperfusion injury and protective effect if ischemic preconditioning. Free Radical Biol. Med. 33, 1200-1208
24. Fernandez, L., Heredia, N., Grande, L., Gomez, G. et al. (2002) Preconditioning protects liver and lung damage in rat liver transplantation: role of xanthine/xanthine oxidase. Hepatology 36, 562-572
25. Peralta, C., Bulbena, O., Xaus, C. et al. (2002) Ischemic preconditioning: a defense mechanism against the reactive oxygen species generated after hepatic ischemia reperfusion. Transplantation 73, 1203-1211
26. Arai, M., Thurman, R. G. and Lemasters, J. J. (2001) Ischemic preconditioning of rat livers against cold storage-reperfusion injury: role of nonparenchymal cells and the phenomenon of heterologous preconditioning. Liver Transplant. 7, 292-299
27. Clavien, P. A., Yadav, S., Sindram, D. and Bentley, R. C. (2000) Protective effects of ischemie preconditioning for liver resection performed under inflow occlusion in humans. Ann. Surg. 232, 155-162
28. 27a Koti, R. S., Yang, W. X., Seifalian, A. M. and Davidson, B. R. (2002) The effect of ischemic preconditioning on hepatic oxygenation, microcirculation and function in a rat model of moderate hepatic steatosis. Gastroenterology 123 (Suppl. S), 86-87
29. Koo, A., Komatsu, H., Tao, G., Inoue, M., Guth, P. H. and Kaplowitz, N. (1992) Contribution of no-reflow phenomenon to hepatic injury after ischemia-reperfusion: evidence for a role for superoxide anion. Hepatology 15, 507-514
30. Seifalian, A. M., Stansby, G. P., Hawkes, D. J., Colchester, A. C. F. and Hobbs, K. E. F. (1991) Measurement of liver blood flow: a review. HPB Surgery 4, 171-186
31. Mastai, R., Laganiere, S., Wanless, I. R., Giroux, L., Rocheleau, B. and Huet, P. M. (1996) Hepatic sinusoidal fibrosis induced by cholesterol and stilbesterol in the rabbit: 2. Haemodynamic and drug disposition studies. Hepatology 24, 865-870
32. Wanless, I. R., Belgiorno, J. and Huet, P. M. (1996) Hepatic sinusoidal fibrosis induced by cholesterol and stilbesterol in the rabbit: 1. Morphology and inhibition of fibrogenesis by dipyridamole. Hepatology 24, 855-964
33. Lee, S. S. and Ho, K. J. (1975) Cholesterol fatty liver. Morphological changes in the course of its development in rabbits. Arch. Pathol. 99, 301-306
34. Seifalian, A. M., El-Desoky, A. and Davidson, B. R. (2001) Hepatic indocyanine green uptake and excretion in a rabbit model of steatosis. Eur. Surg. Res. 33, 193-201
35. Goto, M., Kawano, S., Yoshihara, H. et al. (1992) Hepatic tissue oxygenation as a predictive indicator of ischemia-reperfusion liver injury. Arch. Pathol. Lab. Med. 15, 432-437
36. Sumimoto, K., Inagaki, K., Fukuda, Y., Dohi, K. and Sato, Y. (1987) Significance of graft tissue saturation as a prognostic assessment for orthotopic liver transplantation in the rat. Transplant Proc. 19, 1098-1102
37. Kitai, T., Tanaka, A., Tokuka, A. et al. (1995) Intraoperative measurement of the graft oxygenation state in living related liver transplantation by near infrared spectroscopy. Transplant. Int. 8, 111-118
38. El-Desoky, A., Seifalian, A. M. and Davidson, B. R. (1999) Effect of graded hypoxia on hepatic tissue oxygenation measured by near infrared spectroscopy. J. Hepatol. 31, 71-76
39. 31P nuclear magnetic resonance spectroscopy. FASEB J. 15, 2642-2648
40. Taylor, D. E. and Simonson, S. G. (1996) Use of near-infrared spectroscopy to monitor tissue oxygenation. New Horiz. 4, 420-425
41. Richardson, P. D. I. and Withrington, P. G. (1981) Liver blood flow I. Intrinsic and nervous control of liver blood flow. Gastroentrology 81, 159-173
42. Seifalian, A. M., Mallett, S. V., Rolles, K. and Davidson, B. R. (1997) The hepatic microcirculation during human liver transplantation. Br. J. Surg. 84, 1391-1395
43. Sato, N., Eguchi, H., Inoue, A., Matsumura, T., Kawano, S. and Kamada, T. (1986) Hepatic microcirculation in Zucker fatty rats. Adv. Exp. Med. Biol. 200, 477-483
44. Seifalian, A. M., Chidambaram, V., Rolles, K. and Davidson, B. R. (1998) In vivo demonstration of an impaired microcirculation in steatotic human liver grafts. Liver Trans. Surg. 4, 1-8
45. Teramoto, K., Bowers, J. L., Kruskal, J. B. and Clouse, M. E. (1993) Hepatic microcirculatory changes after reperfusion in fatty and normal liver transplantation in the rat. Transplantation 56, 1076-1082
46. Menger, M. D., Steiner, D. and Messmer, K. (1992) Microvascular ischemia-reperfusion injury in striated muscle: significance of 'no reflow'. Am. J. Physiol. 263, H1892-H1900
47. Menger, M. D., Pelikan, S., Steiner, D. and Messmer, K. (1992) Microvascular ischemia-reperfusion injury in striated muscle: significance of 'reflow paradox'. Am. J. Physiol. 263, H1901-H1906
48. Pannen, B. H., Al Adili, F., Bauer, M., Clemens, M. G. and Geiger, K. K. (1998) Role of endothelins and nitric oxide in hepatic reperfusion injury in the rat. Hepatology 27, 755-764
49. Taneja, C., Prescott, L. and Konery, B. (1998) Critical preservation injury in rat fatty liver is to hepatocytes, not sinusoidal lining cells. Transplantation 65, 167-172
50. Peralta, C., Closa, D., Hotter, G., Gelpi, E., Prats, N. and Rosello-Catafau, J. (1996) Liver ischemic preconditioning is mediated by the inhibitory action of nitric oxide on endothelin. Biochem. Biophys. Res. Commun. 229, 264-270
51. 2 receptors and cyclic adenosine monophosphate to protective ischemic preconditioning of sinusoidal endothelial cells against storage/reperfusion injury in rat livers. Hepatology 32, 297-302
52. Terajima, H., Enders, G., Thiaener, A. et al. (2000) Impact of hyperthermic preconditioning on postischemic hepatic microcirculatory disturbances in an isolated perfusion model of the rat liver. Hepatology 31, 407-415
53. + accumulation and cell killing in isolated rat hepatocytes exposed to hypoxia. Hepatology 31, 166-172
54. Mitsuoka, H., Suzuki, S., Sakaguchi, T. et al. (1999) Contribution of endothelin-1 to microcirculatory impairment in total hepatic ischemia and reperfusion injury. Transplantation 67, 514-520
55. Wang, Y., Mathews, W. R., Guido, D. M., Farhood, A. and Jaeschke, H. (1995) Inhibition of nitric oxide synthesis aggravates reperfusion injury after hepatic ischemia and endotoxemia. Shock 4, 282-288
56. Lemasters, J. J., Stemkowski, C. J., Sungchul, J. I. and Thurman, R. G. (1983) Cell surface changes and enzyme release during hypoxia and reoxygenation in isolated, perfused rat liver. J. Cell Biol. 97, 778-786